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364-365 (2012) 206–211

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Aquaculture

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Increasing hatchery production of juvenile red king ( camtschaticus) through size grading

Benjamin Daly a,⁎, James S. Swingle b, Ginny L. Eckert b a School of and Ocean Sciences, University of Alaska Fairbanks, 201 Railway Avenue, Seward, AK 99664, USA b Juneau Center, School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, 17101 Point Lena Loop Road, Juneau, AK 99801, USA article info abstract

Article history: Cannibalism is problematic in hatchery production of many and can be exacerbated by differen- Received 20 December 2011 tial growth, size variability, and asynchronous molting. We conducted two hatchery experiments in Seward, Received in revised form 23 August 2012 Alaska, USA to investigate effects of size grading on survival and growth of juvenile red king crabs Accepted 23 August 2012 (Paralithodes camtschaticus). We reared larvae and subsequent juveniles until juveniles were eight weeks Available online 31 August 2012 post-settlement. For each experiment, these eight-week old juvenile crabs (approximately 2.0 to 4.5 mm car- apace width) were sorted using a 3.3 mm mesh screen into: “small,”“large,” and “ungraded” size classes. In Keywords: −2 Cannibalism the diet experiment, the three size classes were stocked at a density of 600 crabs m and reared either on a Hatchery control diet of commercial mariculture feeds or the control diet supplemented with astaxanthin and Paralithodes camtschaticus for 53 days. In the density experiment, the three size classes were stocked at densities of 400, 900, and Red king 1400 crabs m−2 and fed the control diet plus astaxanthin and calcium for 31 days. Survival in both experi- Size grading ments was strongly influenced by size grading. Generally, small crabs had higher survival than large and Stock enhancement ungraded crabs. Diet was not a significant factor in weight or survival. Small crabs had relatively high survival at all stocking densities, but all size classes had decreased survival with increasing density, likely from canni- balism. Size graded crabs reared at elevated densities yielded improved biomass per rearing area (g m−2) compared to ungraded populations, suggesting lower survival rates may achieve the goal of optimizing hatchery production. Coupled with appropriate stocking densities, size grading could be used in laboratory and hatchery rearing protocols for red and other likely cannibalistic crustaceans to maximize sur- vival, improve hatchery efficiency, and increase the financial viability of large-scale stock enhancement or aquaculture programs. Published by Elsevier B.V.

1. Introduction field, cannibalism is likely exacerbated by conditions associated with hatchery culture such as artificial diets, high stocking densities, absence Aquaculture-based stock enhancement can be used to sustain or of natural substrates, and elevated temperatures. Improvements in cul- improve fisheries (Leber et al., 2004; Lorenzen et al., 2010); however, turing technology are needed to help overcome cannibalism and im- cannibalism is a bottleneck in the production of juvenile fish and crus- prove the commercial viability of stock enhancement programs. taceans (Aileen et al., 2000; Alston, 1991; Hecht and Appelbaum, Size grading (rearing small and large individuals separately) is com- 1988; Hecht and Pienaar, 1993; Liao et al., 2001; Marshall et al., 2005; monly used in aquaculture of many , including crabs (Marshall et Sotelano et al., 2012; Zmora et al., 2005). Size variation within a cohort al., 2005; Zmora et al., 2005), crayfish (Ahvenharju et al., 2005), fresh- is ubiquitous in fish and aquaculture (see Brett, 1979; water (Daniels and D'Abramo, 1994; Siddiqui et al., 1997; Jobling and Baardvik, 1994; Wickins and Lee, 2002 for a review) and ex- Tidwell et al., 2003), abalone (Heath and Moss, 2009; Mgaya and acerbates cannibalism in the hatchery because of strong resource com- Mercer, 1995), eels (Karipoglou and Nathanailides, 2009), and fish petition among individuals (Karplus et al., 1986) and size hierarchy (Barki et al., 2000; Carmichael, 1994; Wallat et al., 2005)toimprove effects (see Brown, 1946; Koebele, 1985; Magnuson, 1962; Noakes, survival, growth, and feeding efficiency. Size grading reduces aggressive 1978 for a review). Although cannibalism likely occurs naturally in the interactions by disrupting negative effects of dominant, larger compet- itors that suppress the growth and survival of subdominant, smaller in- dividuals (Karplus et al., 1986; Tidwell et al., 2003). Maintaining small ⁎ Corresponding author at: Kodiak Laboratory, Resource Assessment and Conserva- individuals in the population may be important to conserve natural tion Engineering Division, Alaska Fisheries Science Center, National Marine Fisheries genetic and phenotypic variation (Frost et al., 2006), because some indi- Service, NOAA, 301 Research Court, Kodiak, AK 99615, USA. Tel.: +1 907 481 1725; fax: +1 907 481 1701. viduals may have a genetic predisposition for small sizes or slow growth E-mail address: [email protected] (B. Daly). rates (Frost et al., 2006; Gu et al., 1995). The genetic contribution of

0044-8486/$ – see front matter. Published by Elsevier B.V. http://dx.doi.org/10.1016/j.aquaculture.2012.08.034 B. Daly et al. / Aquaculture 364-365 (2012) 206–211 207 those individuals would be reduced if hatcheries select against slow 2.3. Size grading growers. Regular size grading may increase survival or growth rates of smaller individuals from compensatory effects (Jobling, 2010; Ricker, After the eight-week nursery grow-out period, crabs exhibited a size 1979). range of approximately 2.0 to 4.5 mm carapace width (CW). We Most crab and stock enhancement programs require hun- collected crabs from mass rearing nursery tanks and sorted by size dreds of thousands or even millions of individuals for release (Aiken using a 3.3 mm mesh screen. We sorted equal numbers of crabs and Waddy, 1995; Bannister and Addison, 1998; Comeau, 2006; Secor (~100) at a time to standardize any potential physical damage. Crabs et al., 2002; Stevens, 2006a,b; Zohar et al., 2008). In Japan, annual pro- that fell through the screen are referred to as “small”, while crabs duction of juvenile swimming crabs ( trituberculatus)isap- retained on top of the screen are referred to as “large”. The ungraded proximately 60 million with yearly releases ranging from 28 to 42 treatment represented approximately 50% small and 50% large crabs. million (Secor et al., 2002). Stock enhancement has been proposed as a possible population recovery tool for depressed (Paralithodes camtschaticus) stocks in Alaska, USA and will likely also re- 2.4. Limb loss quire annual releases of millions to support a viable fishery (Stevens, 2006b). Hatchery production of juvenile red king crabs is limited by To determine physical effects of the sorting process, we collected cannibalism and slow growth, which can be mediated with artificial 100 pre-sorted crabs from the nursery tanks and examined them for substrates, diet modification, and temperature (Borisov et al., 2007; missing limbs. The same crabs were then sorted by size using screens Daly et al., 2009, 2012; Long et al., 2012; Stevens and Swiney, 2005; (described above) and reexamined for limb loss. The numbers of Stoner, 2009; Stoner et al., 2010a,b). Additional rearing technologies crabs with at least one missing limb and the total number of missing must be developed for a large-scale stock enhancement program to be limbs per crab were recorded. The limb loss assessment was replicat- economically feasible. This study aimed to determine the effects of ed three times. size grading by investigating survival and growth of size-graded juve- nile red king crab reared using different diets and stocking densities. 2.5. Experiment 1: diet and size grading effects 2. Materials and methods We initiated the first experiment in summer 2009 after the 2.1. Broodstock and larval rearing eight-week nursery grow-out period. Two factors (three size-grading treatments and two diet treatments) resulted in six treatments that Twenty ovigerous females were captured with baited commercial were each replicated six times. Crabs were sorted into small, large, pots in Bristol Bay, Alaska during November 2008 and 2009 for experi- and ungraded size classes as described above. Crabs were stocked at ments the following spring and summer. Crabs were transported to the 600 crabs m−2 in flat bottomed 58 cm tall by 58 cm diameter cylindri- Alutiiq Pride Shellfish Hatchery in Seward, Alaska, and placed in 2000 L cal containers with a 100 μm mesh screen on the bottom, a surface area tanks containing flow-through ambient seawater and each fed 20 g of approximately 0.25 m2, and volume of approximately 65 L, hereafter chopped herring and squid twice per week. Once hatching began called silos. Nine silos were placed in each of four larger 3200 L rectan- (April 2009 and 2010), larvae from eight females were mixed and raised gular tanks and treatment replicates were randomly assigned among in 1200 L cylindrical tanks until the first juvenile instar (C1) stage. Zoeal tanks. All silos contained equal amounts (approximately 100 g larvae were daily fed San Francisco Bay strain Artemia nauplii, which (0.88 m2)) of commercial fishing gillnet (7.6 cm mesh size). The gillnet were enriched with DC DHA Selco® (INVE Aquaculture, UT, USA) twine consisted of nine woven nylon monofilaments for a total enrichment media in 100 L cylindrical tanks for 24 h. diameter of approximately 1.0 mm and surface area of 88 cm2 g−1. Gillnet improves survival by providing complex structure with intersti- 2.2. Nursery grow-out tial spaces reducing crab contact with each other (Daly et al., 2009). All silos were supplied with flow-through ambient seawater entering from We collected recently-settled, first stage (C1) juvenile crabs from the top with a flow rate of approximately 1.5 L min−1. Incoming larval rearing tanks, mixed them randomly and mass reared them in seawater was sourced from a deep-water (~75 m) intake at ambient three 2000 L cylindrical nursery tanks for eight weeks. Nursery tanks temperature and was filtered to 5 μm, UV sterilized, and carbon filtered. contained artificial seaweed and commercial fishing gillnet (7.6 cm Temperatures ranged from approximately 8 °C to 12 °C. mesh size) to reduce agonistic interactions among conspecifics (Daly Crabs were fed the control diet (described above) and the control et al., 2009). Crabs were fed the control diet approximately 2% body diet supplemented with astaxanthin and calcium. Astaxanthin dry weight daily and excess feed and wastes were removed weekly. improves survival and growth of hatchery-cultured juvenile red king The control diet consisted of Cyclop-eeze® (Argent Chemical Laborato- crabs (Daly et al., 2012), and additional calcium may enhance growth ries, WA, USA), Otohime B1 and B2 (Reed Mariculture, CA, USA), frozen or survival as observed in other species (Hossain and Furuichi, 2000a, enriched Artemia nauplii, and Zeigler™ feed (Zeigler Bros, Inc., b). Supplements consisted of two ground cuttlebones (~12 g each) PA, USA). Each feed type was alternated daily. Cyclop-eeze® is a frozen and 2 g dry powdered NatuRose™ (1.5% pure astaxanthin) mixed copepod (~800 μm length) high in carotenoids and omega-3 highly with 25 g Zeigler™ shrimp feed and 25 g Otohime B1 and bound with unsaturated fatty acids (HUFAs). Otohime B is a high protein diet devel- 2 egg whites (~35 g each). Once bound with egg whites, supplements oped for marine fish and consists of 200–360 μm (B1) and 360–620 μm were ground producing particles approximately 400–1000 μm. Supple- (B2) sinking pellets. Newly hatched San Francisco Bay strain Artemia ments were administered in lieu of the control diet twice weekly. Crabs nauplii (~450 μm length) have high levels of lipids and unsaturated were fed approximately 2% body dry weight daily and excess feed and fatty acids (Tizol-Correa et al., 2006). Artemia nauplii were enriched waste were removed weekly. with DC DHA Selco® (INVE Aquaculture, UT, USA) enrichment media The duration of the experiment was 53 days to allow crabs to molt for 24 h to enhance their nutritional quality and then frozen. The frozen at least once (Stoner et al., 2010a). Survival was assessed by counting enriched Artemia nauplii (~750 μm length) were negatively buoyant all crabs within each replicate at the start and end of the experiment. and available for benthic crab consumption. Zeigler™ PL Redi-Reserve Growth was assessed by weighing to the nearest 0.01 g (blotted wet commercial shrimp feed (400–600 μm particles) is commonly used in weight) ten randomly selected crabs from each replicate at the end of crustacean aquaculture due to its high levels of Highly Unsaturated the experiment. Exuvia were examined to determine when molting Fatty Acids (Meade and Watts, 1995). to the next instar stage occurred. 208 B. Daly et al. / Aquaculture 364-365 (2012) 206–211

2.6. Experiment 2: stocking density and size grading effects marginally higher survival (58.0±3.7%) compared to crabs fed the control diet (50.9±4.7%, Tukey's HSD, p=0.068). Diet did not impact We initiated the second experiment in summer 2010 after the weight for small (t=−0.452, df=58, p=0.653), large (t=−0.954, eight-week nursery grow-out period. Crabs were size-graded as in df=58, p=0.344), or ungraded (t=−0.338, df=58, p=0.736) Experiment 1. Crabs were placed in silos within rectangular tanks crabs. (described above) at densities of 400, 900, and 1400 crabs m−2. Two factors (size-grading and density) were varied resulting in nine 3.3. Experiment 2: stocking density and size grading effects treatments that were each replicated four times. One treatment repli- cate was assigned to a randomly selected silo in each of the four rect- Survival varied significantly by size-grading class and density with angular tanks. Crabs were fed the aforementioned diet containing a significant size-grading class∗density interaction (Table 2, Fig. 2). astaxanthin and calcium supplements and reared at temperatures The significant interaction reveals that survival of the size grading ranging from approximately 11 °C to 14 °C. classes was affected differentially by density. Increasing densities Experiment two was shorter in duration (31 days) due to a seawa- resulted in declining survival for all size grading classes (Fig. 2, ter pump malfunction; however, the warmer rearing temperature in Tukey's HSD, pb0.05). Survival of large crabs at low density (93.5± 2010 likely allowed for crabs to molt at least once. Survival was 3.2%) was greater than survival of ungraded crabs at low density assessed by counting all crabs within each replicate at the start and (65.3±7.1%, Tukey's HSD, pb0.001), but there was no difference in end of the experiment. Because of the seawater pump malfunction, survival between these two size classes at moderate (Tukey's HSD, crabs needed to be quickly moved to an alternate location. As such, p=0.144) and high densities (Tukey's HSD, p=0.294) (Fig. 2). growth was assessed by weighing (blotted wet weight) all crabs Weight increased significantly with density for large crabs (ANOVA, within the same silo to give an aggregate total crab weight for each pb0.001), but not small (ANOVA, p=0.239) or ungraded crabs silo to save time. The total crab weight was then divided by the (ANOVA, p=0.086) (Table 2, Fig. 3). Crab biomass (g m−2) de- total number of crabs within the silo to yield the average crab weight creased with survival for all crab size classes (Fig. 4A, Table 3). At to the nearest 0.01 g. the end of the experiment, crab biomass (g m−2) increased with the final crab density (crabs m−2) for small and ungraded crabs; 2.7. Statistical analysis however, crab biomass (g m−2) decreased with the final crab density (crabs m−2) for large crabs (Fig. 4B, Table 3). A paired t-test was used to determine significance in limb loss among pre- and post-sorted crabs. Two-way ANOVA and post-hoc 4. Discussion comparisons (Tukey's HSD) on arcsine square root transformed data were used to compare survival among treatments for both experi- Small crabs had relatively high survival and can be held at elevat- ments. Weight data in experiment one were log transformed to ed stocking densities without significant mortality compared to large meet assumptions of normality and equal variance. An unpaired and ungraded crabs. Differential survival rates likely resulted from t-test was used to compare weight between diets for each of the size-related differences in behavior. Small red king crabs exhibit cryp- three size classes in the first experiment. One-way ANOVA and tic behavior and seek habitats with structural complexity (Pirtle and post-hoc comparisons (Tukey's HSD) were used to compare weight Stoner, 2010; Stevens and Swiney, 2005; Stoner, 2009), while rela- among the three densities for each size class in the second experiment. tively larger juveniles become increasingly active in food searches, Linear regression analysis was used to relate survival and resultant rear- predator response, and agonistic behavior with conspecifics (Pirtle −2 −2 ing density (crabs m ) to crab biomass (g m ) using models: crab and Stoner, 2010; Stoner et al., 2010b; B. Daly, pers. obs.) suggesting biomass=A+(B∗survival); crab biomass=A+(B∗density). All anal- that there is a gradient in behavior with size. Size-grading, by remov- yses were conducted using Sigma Stat v.4 (Aspire Software Internation- ing large, dominant crabs likely reduced competition for food, dam- al, Ashburn, VA, USA). Significance for all tests was established with age from aggressive interactions, and predation; while the cryptic α=0.05. and more docile nature of small crabs likely facilitates high density holding due to reduced encounter rates. Increased activity of large 3. Results and ungraded crabs may elevate agonistic interactions or cannibal- ism, especially at higher stocking densities. Cannibalism is wide- 3.1. Limb loss spread in the kingdom (Fox, 1975; Polis, 1981) including many decapod crustacean species (Fernández et al., 1993; Hines et The sorting process did not increase limb loss significantly in terms of al., 1990; Kurihara and Okamoto, 1987; Lovrich and Sainte-Marie, percentage of crabs with at least one missing limb and the average num- 1997; Mansour and Lipcius, 1991; Marshall et al., 2005; Sotelano et ber of missing limbs per crab (t=−2.392, df=2, p=0.139 for % missing al., 2012), thus juvenile red king crabs may initiate cannibalism to −1 limbs; t=−1.596, df=2, p=0.252 for missing limbs crab ). Prior to eliminate competitive counterparts when resources (i.e., space, refuge sorting, 22.7±2.0% (average±SE) of the crabs had at least one missing availability) are limiting. limb and 29.7±4.0% had missing limbs after sorting. Crabs had 0.31± Recently molted crabs are at greatest risk of being cannibalized 0.021 missing limbs prior to sorting and 0.39±0.064 missing limbs because of reduced mobility and lack of defensive armor. For after sorting.

3.2. Experiment 1: diet and size grading effects Table 1 Experiment 1: Two-way ANOVA for survival of red king crab (P. camtschaticus) juveniles Average (±SE) survival to day 53 across all treatments was 54.4± reared for 53 days with three size-grading classes (small, large, and ungraded) and two fi 3.0%. Survival varied significantly among size-grading classes and diets (control and control plus astaxanthin and calcium). Bold indicates statistical signi - cance (α≤0.05). marginally significantly between diets and there were no significant size-grading class∗diet interactions (Table 1). Small crabs had higher Effect SS df MS F p survival (73.6±3.5%) than large (50.9±2.4%, Tukey's HSD, pb0.001) Survival Size 0.851 2 0.425 32.20 b0.001 and ungraded crabs (38.9±3.6%, Tukey's HSD, pb0.001) (Fig. 1). Diet 0.047 1 0.047 3.58 0.068 Large crabs had higher survival than ungraded crabs (Tukey's HSD, Size×diet 0.032 2 0.016 1.22 0.311 p=0.024). Crabs fed calcium and astaxanthin supplements had Residual 0.396 30 0.013 B. Daly et al. / Aquaculture 364-365 (2012) 206–211 209

Fig. 1. Experiment 1: Average (±SE) percent survival of small, large, and ungraded juvenile red king crabs fed either the control diet or the control diet enriched with Fig. 2. Experiment 2: Average (±SE) percent survival of small, large, and ungraded −2 calcium and astaxanthin. Different letters indicate statistical significance (Tukey's juvenile red king crabs reared at 400, 900, and 1400 crabs m . Different letters indicate fi ≤ HSD, p≤0.05). statistical signi cance (Tukey's HSD, p 0.05).

blue-swimmer crabs (Portunus pelagicus), victims of cannibalism are experiments, but the longer experiment (Exp 1: 53 days) likely recently molted and smaller than consumers, suggesting that transi- allowed a higher proportion of crabs to molt multiple times. Culturing tional stages associated with ecdysis are especially vulnerable juvenile red king crabs at elevated temperatures does not decrease (Marshall et al., 2005). Early juvenile red king crabs (C1–C3) have rel- condition or nutritional status (Stoner et al., 2010a) suggesting bene- atively synchronous molt timing, while molting patterns become in- fits of temperature-mediated growth if cannibalism is minimized. creasingly asynchronous with time, which can cause a divergence in Large crabs had lower survival but greater end weight at higher body size (Westphal, 2011; B. Daly and J. Swingle, pers. obs.). Because stocking densities, which may result from competitive growth effects, crabs were held in populations, we cannot be certain if the observed enhanced feeding from social facilitation (Kurta, 1982), or size selec- size discrepancy among size classes is caused by variability in molting tive predation on relatively smaller individuals. Additionally, greater frequency or molt increment. For example, relatively small crabs may cannibalism may have increased nutritional intake and growth of have similar molt frequencies as larger crabs of the same age, but the survivors; however, uneaten food was present and evenly dis- have comparatively small molt increments. The degree of cannibalism persed in all treatments indicating food was not limiting and equally in wild red king crab populations is unknown; however, we expect available to all individuals. Density and diet dependent growth have that high density hatchery-cultured crabs have much higher rates of been reported in previous studies using ungraded juvenile red king cannibalism than what might be experienced in the wild. crabs (Daly et al., 2009, 2012); however, the present study demon- Generally, crustacean metabolic demand is coupled with temper- strated growth did not increase in small-sized or ungraded crabs at ature resulting in increased feeding and growth (molt frequency, higher densities or with dietary supplements in any size treatment, molt increment) with increasing temperature (Hartnoll, 1982, suggesting that some crabs may have a genetic predisposition for 2001). Recently-settled red king crab have a wide range of thermal slow growth regardless of diet and lack of competition from larger tolerance (Stoner et al., 2010a); however, cannibalism is exacerbated conspecifics. Further research is needed to investigate the possibility with increasing temperature (Stoner et al., 2010b) likely from greater of genetic predisposition for slow growth. Because of possible genetic vulnerability associated with molting. Rearing temperatures in the effects, we conclude that size grading is important for preserving a present study (Exp 1: 8–12 °C; Exp 2: 11–14 °C) were likely warm range of size classes, even when coupled with other rearing technol- relative to temperatures experienced by wild red king crab juveniles ogies such as optimal diet and increased structures. in northern areas (e.g., Norton Sound, Bristol Bay) but may represent Cannibalism in other species often occurs to meet metabolic de- temperatures in the Gulf of Alaska (e.g., Kodiak, Southeast Alaska). mands when food is limiting (Elgar and Crespi, 1992); however, juve- Because cannibalism is high during molting, rearing temperature nile red king crabs exhibited cannibalism even when food was and experimental duration likely impacted our results. We estimate administered in excess. We report a marginally non-significant in- that crabs molted between one and three times during both crease in survival with astaxanthin and calcium supplementation. Previous studies with astaxanthin supplementation showed im- proved survival and shell coloration of ungraded red king crabs, suggesting astaxanthin provides some nutritional benefit(Daly et fi fi Table 2 al., 2012). Bene ts of supplements may be ampli ed for ungraded Experiment 2: Two-way ANOVA for survival and one-way ANOVAs for weight of red crabs if subdominant individuals cannot obtain adequate nutrition king crab (P. camtschaticus) juveniles reared for 31 days among three size-grading clas- with commercial feeds alone. Size grading may stabilize hierarchical −2 ses (small, large, and ungraded) and three densities (400, 900, and 1400 crabs m ). structures and ease dominance pressure allowing crabs to feed satis- Bold indicates statistical significance (α≤0.05). factorily in the absence of larger individuals. Astaxanthin is likely a Effect SS df MS F p natural dietary component of red king crab because it is synthesized Survival Size 1.908 2 0.954 80.27 b0.001 by microalgae and bio-accumulates throughout marine food webs Density 1.872 2 0.936 78.76 b0.001 (Harmon and Cysewski, 2008). As such, astaxanthin supplementation Size×density 0.629 4 0.157 13.23 b0.001 should be included in hatchery diets especially in the absence of size Residual 0.321 27 0.012 grading. Weight (small) Density 46.5 2 23.2 1.69 0.239 Residual 123.8 9 13.8 Size grading allows for greater hatchery production of juvenile red Weight (large) Density 37,060 2 18,530 51.47 b0.001 king crabs compared to mixed populations and should be used in fu- Residual 3240 9 360 ture rearing protocols in combination with other technologies such as Weight (ungraded) Density 4835 2 2418 3.26 0.086 artificial substrates, optimal diets, and appropriate stocking densities. Residual 6684 9 743 Depending on project goals (total biomass or number of individuals), 210 B. Daly et al. / Aquaculture 364-365 (2012) 206–211

Fig. 4. Experiment 2: Linear regression between crab biomass (g m−2) and (A) survival and (B) resultant rearing density (crabs m−2) for small, large, and ungraded juvenile red king crabs. See parameter estimates in Table 3.

Table 3 Parameter estimates for linear regressions relating crab biomass (g m−2)tosurvivaland resultant rearing density (crabs m−2). Crab biomass=A+(B∗survival); Crab biomass= A+(B∗density), where A and B are parameters. Bold indicates statistical significance (α≤0.05).

Parameters R2 p Fig. 3. Experiment 2: Average (±SE) individual weight of (A) small, (B) large, and − AB (C) ungraded juvenile red king crabs reared at 400, 900, and 1400 crabs m 2. Different letters indicate statistical significance (Tukey's HSD, p≤0.05). Survival Small 116.78 −0.988 0.403 0.027 Large 47.37 −0.249 0.842 b0.001 Ungraded 45.51 −0.382 0.605 0.003 Density Small 2.39 0.035 0.945 b0.001 Large 67.44 −0.108 0.644 0.002 lower survival rates may achieve the goal of maximizing hatchery Ungraded 11.87 0.050 0.254 0.095 production (Ut et al., 2007; Zmora et al., 2005), especially when con- sidering rearing effort, utilization of hatchery space, and economic cost. For example, small crabs can be held at higher densities and achieve higher survival (numbers of individuals) and biomass per Pride Shellfish Hatchery. The authors would like to thank H. McCarty, −2 rearing space (g m ) in the absence of large individuals, while rear- R. Painter, J. Stephan, and L. Dochterman for helping with broodstock ing large crabs separately at moderate and high densities allows for acquisition, J. Christiansen for project assistance, and J. Hetrick for higher biomass per rearing space despite lower survival, compared hatchery logistical support. Three anonymous reviewers provided to ungraded crabs. However, if the goal is to optimize total numbers helpful comments which greatly improved the manuscript. of individuals produced, stocking densities should be adjusted by crab size. For example, small crabs can be held at high densities with low mortality rates, while densities must be reduced for larger References juveniles. For red king crab stock enhancement, the optimal size for Ahvenharju, T., Savolainen, R., Tulonen, J., Ruohonen, K., 2005. Effects of size grading on release is unknown and may require long-term hatchery grow-out. growth, survival, and cheliped injuries of signal crayfish ( leniusculus Improving nursery techniques can boost the productivity and finan- Dana) summerlings (age 0+). Aquaculture Research 36, 857–867. cial viability of a large-scale stock enhancement program. Aiken, D.E., Waddy, S.L., 1995. Aquaculture. In: Factor, J.R. (Ed.), of the , Homarus americanus. Academic Press, New York, pp. 153–176. Aileen, T.S.-H., Zulfigar, B.Hj.Y., Fujii, Y., Fukuda, T., Terazaki, M., 2000. JSPS/UCC Report: Acknowledgments Culture of Japanese Blue Crab (). The Center of Internation- al Cooperation, The Ocean Research Institute, University of Tokyo (29 pp.). Alston, D.E., 1991. Culture of crustaceans in the Caribbean. World Aquaculture 22, 64–69. This work was funded by a NOAA Aquaculture award to Alaska Sea Bannister, R.C.A., Addison, J.T., 1998. Enhancing lobster stocks: a review of recent European Grant College Program, University of Alaska Fairbanks and Alutiiq methods, results, and future prospects. Bulletin of Marine Science 62, 369–387. B. Daly et al. / Aquaculture 364-365 (2012) 206–211 211

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